A common neural code for perceived and inferred emotion.

Amy E Skerry, Rebecca Saxe
Author Information
  1. Amy E Skerry: Department of Psychology, Harvard University, Cambridge, Massachusetts 02138, and amy.skerry@gmail.com.
  2. Rebecca Saxe: Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139.

Abstract

Although the emotions of other people can often be perceived from overt reactions (e.g., facial or vocal expressions), they can also be inferred from situational information in the absence of observable expressions. How does the human brain make use of these diverse forms of evidence to generate a common representation of a target's emotional state? In the present research, we identify neural patterns that correspond to emotions inferred from contextual information and find that these patterns generalize across different cues from which an emotion can be attributed. Specifically, we use functional neuroimaging to measure neural responses to dynamic facial expressions with positive and negative valence and to short animations in which the valence of a character's emotion could be identified only from the situation. Using multivoxel pattern analysis, we test for regions that contain information about the target's emotional state, identifying representations specific to a single stimulus type and representations that generalize across stimulus types. In regions of medial prefrontal cortex (MPFC), a classifier trained to discriminate emotional valence for one stimulus (e.g., animated situations) could successfully discriminate valence for the remaining stimulus (e.g., facial expressions), indicating a representation of valence that abstracts away from perceptual features and generalizes across different forms of evidence. Moreover, in a subregion of MPFC, this neural representation generalized to trials involving subjectively experienced emotional events, suggesting partial overlap in neural responses to attributed and experienced emotions. These data provide a step toward understanding how the brain transforms stimulus-bound inputs into abstract representations of emotion.

Keywords

References

  1. Front Hum Neurosci. 2013 Oct 28;7:692 [PMID: 24194707]
  2. Neuroimage. 2011 Mar 15;55(2):705-12 [PMID: 21182967]
  3. Neuropsychologia. 2009 Dec;47(14):3059-66 [PMID: 19596021]
  4. Neuroimage. 2009 Jan 15;44(2):569-80 [PMID: 18852053]
  5. Soc Cogn Affect Neurosci. 2014 Sep;9(9):1289-302 [PMID: 23887811]
  6. Neuroimage. 2006 Apr 1;30(2):580-7 [PMID: 16275138]
  7. Neuroimage. 2006 Jan 1;29(1):90-8 [PMID: 16122944]
  8. Trends Cogn Sci. 2013 Aug;17(8):401-12 [PMID: 23876494]
  9. J Vis. 2010;10(5):11 [PMID: 20616141]
  10. Science. 1993 Oct 29;262(5134):685-8 [PMID: 8235589]
  11. Psychol Sci. 2008 Apr;19(4):399-404 [PMID: 18399894]
  12. Cereb Cortex. 2005 Dec;15(12):1866-76 [PMID: 15746001]
  13. J Vis. 2010;10(14). pii: 36. doi: 10.1167/10.14.36 [PMID: 21196514]
  14. Science. 2001 Sep 28;293(5539):2425-30 [PMID: 11577229]
  15. Emotion. 2009 Feb;9(1):128-33 [PMID: 19186926]
  16. Emotion. 2009 Aug;9(4):478-87 [PMID: 19653768]
  17. Neuroimage. 2009 Feb 1;44(3):1210-23 [PMID: 18973818]
  18. Trends Cogn Sci. 2006 Sep;10(9):424-30 [PMID: 16899397]
  19. Neuroimage. 2012 May 1;60(4):2357-64 [PMID: 22398396]
  20. Neuropsychologia. 2011 Apr;49(5):992-8 [PMID: 21281653]
  21. Neuroimage. 2012 Feb 1;59(3):3050-9 [PMID: 22019857]
  22. Neuroimage. 2013 Aug 1;76:412-27 [PMID: 23507394]
  23. Neuroimage. 2003 Aug;19(4):1273-302 [PMID: 12948688]
  24. Trends Cogn Sci. 2007 Aug;11(8):333-41 [PMID: 17631409]
  25. Curr Opin Neurobiol. 2002 Apr;12(2):169-77 [PMID: 12015233]
  26. PLoS One. 2013;8(9):e75468 [PMID: 24073267]
  27. Neuroimage. 2010 Feb 1;49(3):1943-8 [PMID: 19285144]
  28. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10749-53 [PMID: 8248166]
  29. Neuroimage. 2008 Oct 15;43(1):44-58 [PMID: 18672070]
  30. J Neurosci. 2009 Sep 30;29(39):12315-20 [PMID: 19793990]
  31. Trends Cogn Sci. 2011 Feb;15(2):85-93 [PMID: 21167765]
  32. Behav Brain Sci. 2012 Jun;35(3):121-43 [PMID: 22617651]
  33. Science. 2007 May 18;316(5827):1002-5 [PMID: 17510358]
  34. Nat Neurosci. 2005 May;8(5):679-85 [PMID: 15852014]
  35. Psychol Sci. 2011 Nov;22(11):1359-66 [PMID: 22006061]
  36. J Neurophysiol. 2007 Feb;97(2):1671-83 [PMID: 17093126]
  37. Proc Natl Acad Sci U S A. 2012 Dec 26;109(52):E3640-8 [PMID: 23184972]
  38. Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11382-7 [PMID: 19549849]
  39. Curr Biol. 2007 Jan 9;17(1):20-5 [PMID: 17208181]
  40. Exp Brain Res. 2008 Dec;191(4):383-402 [PMID: 18936922]
  41. Philos Trans R Soc Lond B Biol Sci. 2006 Dec 29;361(1476):2109-28 [PMID: 17118927]
  42. Neuropsychologia. 2012 Jan;50(2):219-31 [PMID: 22154962]
  43. J Neurosci. 2013 Nov 27;33(48):18906-16 [PMID: 24285896]
  44. Neuroimage. 2013 Jan 15;65:69-82 [PMID: 23041526]
  45. Neuron. 2012 Feb 9;73(3):415-34 [PMID: 22325196]
  46. Brain. 2009 Mar;132(Pt 3):617-27 [PMID: 18971202]
  47. Curr Biol. 2011 Nov 8;21(21):1817-21 [PMID: 22036180]
  48. J Neurosci. 2012 Nov 7;32(45):15952-62 [PMID: 23136433]
  49. J Neurosci. 2007 Sep 12;27(37):9984-8 [PMID: 17855612]
  50. Front Syst Neurosci. 2010 Mar 15;4:6 [PMID: 20305753]
  51. J Neurosci. 2011 Mar 30;31(13):4792-804 [PMID: 21451017]
  52. PLoS One. 2013;8(3):e58166 [PMID: 23483988]
  53. Nat Rev Neurosci. 2006 Apr;7(4):268-77 [PMID: 16552413]
  54. Nat Rev Neurosci. 2014 Aug;15(8):549-62 [PMID: 24986556]
  55. Neuropsychologia. 2006;44(3):374-83 [PMID: 16112148]
  56. J Cogn Neurosci. 2003 Apr 1;15(3):324-37 [PMID: 12729486]
  57. Cognition. 2005 Jan;94(3):193-213 [PMID: 15617671]
  58. Nat Rev Neurosci. 2010 Nov;11(11):773-83 [PMID: 20959860]
  59. J Autism Dev Disord. 2001 Feb;31(1):5-17 [PMID: 11439754]
  60. Nat Neurosci. 2001 Jan;4(1):17-8 [PMID: 11135640]
  61. J Neurosci. 2010 Jul 28;30(30):10127-34 [PMID: 20668196]
  62. Neuroimage. 2011 Jun 15;56(4):2356-63 [PMID: 21473921]
  63. J Psychiatry Neurosci. 2009 Nov;34(6):418-32 [PMID: 19949718]
  64. Neuroimage. 2009 Mar;45(1 Suppl):S199-209 [PMID: 19070668]
  65. Soc Cogn Affect Neurosci. 2012 Mar;7(3):274-81 [PMID: 21427193]
  66. J Neurosci. 2014 Jul 2;34(27):9173-7 [PMID: 24990937]
  67. Nat Neurosci. 2014 Aug;17(8):1114-22 [PMID: 24952643]
  68. Trends Cogn Sci. 2009 Aug;13(8):334-40 [PMID: 19643659]
  69. Cognition. 1998 Jul;67(1-2):21-44 [PMID: 9735535]
  70. Neuroimage. 2003 Aug;19(4):1835-42 [PMID: 12948738]
  71. Neural Comput. 2006 Aug;18(8):1951-86 [PMID: 16771659]
  72. Science. 2005 Nov 4;310(5749):863-6 [PMID: 16272124]
  73. J Neurosci. 2010 Jun 23;30(25):8481-8 [PMID: 20573895]
  74. J Neurosci. 2013 Jun 19;33(25):10552-8 [PMID: 23785167]
  75. Cereb Cortex. 2014 Aug;24(8):1988-95 [PMID: 23463339]
  76. Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3863-8 [PMID: 16537458]
  77. Philos Trans R Soc Lond B Biol Sci. 2009 May 12;364(1521):1309-16 [PMID: 19528012]
  78. Ann N Y Acad Sci. 2009 Jun;1167:16-30 [PMID: 19580548]
  79. J Neurosci. 2013 Jul 3;33(27):11032-9 [PMID: 23825408]
  80. Nat Neurosci. 2007 Dec;10(12):1625-33 [PMID: 17982449]

Grants

  1. R01 MH096914/NIMH NIH HHS
  2. 1R01 MH096914-01A1/NIMH NIH HHS

MeSH Term

Adult
Brain
Emotions
Female
Humans
Magnetic Resonance Imaging
Male
Nerve Net
Photic Stimulation
Pilot Projects
Psychomotor Performance
Young Adult

Word Cloud

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